Global transcriptome analysis of Atlantic cod (Gadus morhua) liver after in vivo methylmercury exposure suggests effects on energy metabolism pathways

Aquatic Toxicology

Volumn 126, Issue , 2013, Pages 314-325

  Yadetie, Fekadu ^a   Karlsen, Odd Andre ^a   Lanzén, Anders ^a   Berg, Karin ^a   Olsvik, Pål ^b   Hogstrand, Christer ^c   Goksøyr, Anders ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b INSTITUTE OF MARINE RESEARCH   (Norway)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Atlantic cod; Biomarker; Methylmercury; Microarray; Toxicogenomics; Transcription

Indexed keywords

AMINO ACID; BIOLOGICAL MARKER; FATTY ACID; GLUCOSE; GLUTATHIONE; METHYLMERCURY; SULFUR; TRANSCRIPTION FACTOR NRF2;

AMINO ACID; AQUATIC ENVIRONMENT; BIOMARKER; DEMERSAL FISH; ENZYME; FATTY ACID; FOOD CONSUMPTION; GLUCOSE; HEALTH RISK; METABOLISM; METHYLMERCURY; PHYSIOLOGICAL RESPONSE; POLLUTION EXPOSURE; PROTEOMICS; TOXICITY;

AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATLANTIC COD; CONTROLLED STUDY; CYTOSKELETON; CYTOSKELETON REMODELING; DNA MICROARRAY; ENERGY METABOLISM; ENZYME INDUCTION; FATTY ACID METABOLISM; FATTY ACID OXIDATION; FEMALE; GENE CONTROL; GENE FUNCTION; GENE IDENTIFICATION; GENETIC CODE; GLUCOSE METABOLISM; GLUTATHIONE METABOLISM; IMMUNE RESPONSE; LIVER; LONG TERM EXPOSURE; MALE; NONHUMAN; OXIDATIVE STRESS; POLLUTION MONITORING; PRIORITY JOURNAL; REGULATORY MECHANISM; TRANSCRIPTOMICS;

ANIMALS; ENERGY METABOLISM; FISH PROTEINS; GADUS MORHUA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LIVER; METHYLMERCURY COMPOUNDS; OXIDATIVE STRESS; WATER POLLUTANTS, CHEMICAL;

GADUS MORHUA;

EID: 84871791305     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.09.013     Document Type: Article

References (75)

1. Amlund H., Lundebye A.-K., Berntssen M.H.G. Accumulation and elimination of methylmercury in Atlantic cod (Gadus morhua L.) following dietary exposure. Aquatic Toxicology 2007, 83:323-330.
2. Bakir F., Damluji S.F., Aminzaki L., Murtadha M., Khalidi A., Alrawi N.Y., Tikriti S., Dhahir H.I., Clarkson T.W., Smith J.C., Doherty R.A. Methylmercury poisoning in Iraq: an interuniversity report. Science 1973, 181:230-241.
3. Balk L., Hylland K., Hansson T., Berntssen M.H.G., Beyer J., Jonsson G., Melbye A., Grung M., Torstensen B.E., Borseth J.F., Skarphedinsdottir H., Klungsøyr J. Biomarkers in natural fish populations indicate adverse biological effects of offshore oil production. PLoS One 2011, 6(5):e19735.
4. Bateman A., Birney E., Cerruti L., Durbin R., Etwiller L., Eddy S.R., Griffiths-Jones S., Howe K.L., Marshall M., Sonnhammer E.L.L. The Pfam protein families database. Nucleic Acids Research 2002, 30:276-280.
5. Bauer M., Hamm A.C., Bonaus M., Jacob A., Jaekel J., Schorle H., Pankratz M.J., Katzenberger J.D. Starvation response in mouse liver shows strong correlation with life-span-prolonging processes. Physiological Genomics 2004, 17:230-244.
6. Berg K., Puntervoll P., Valdersnes S., Goksøyr A. Responses in the brain proteome of Atlantic cod (Gadus morhua) exposed to methylmercury. Aquatic Toxicology 2010, 100:51-65.
7. Bloom N.S. On the chemical form of mercury in edible fish and marine invertebrate tissue. Canadian Journal of Fisheries and Aquatic Sciences 1992, 49:1010-1017.
8. Bohne-Kjersem A., Skadsheim A., Goksøyr A., Grøsvik B.E. Candidate biomarker discovery in plasma of juvenile cod (Gadus morhua) exposed to crude North Sea oil, alkyl phenols and polycyclic aromatic hydrocarbons (PAHs). Marine Environmental Research 2009, 68:268-277.
9. Booman M., Borza T., Feng C.Y., Hori T.S., Higgins B., Culf A., Leger D., Chute I.C., Belkaid A., Rise M., Gamperl A.K., Hubert S., Kimball J., Ouellette R.J., Johnson S.C., Bowman S., Rise M.L. Development and experimental validation of a 20K Atlantic Cod (Gadus morhua) oligonucleotide microarray based on a collection of over 150,000 ESTs. Marine Biotechnology 2011, 13:733-750.
10. Bridges C.C., Zalups R.K. Transport of inorganic mercury and methylmercury in target tissues and organs. Journal of Toxicology and Environmental Health-Part B: Critical Reviews 2010, 13:385-410.
11. Brown M.S., Goldstein J.L. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 1997, 89:331-340.
12. Burger J., Gochfeld M. Risk to consumers from mercury in Pacific cod (Gadus macrocephalus) from the Aleutians: fish age and size effects. Environmental Research 2007, 105:276-284.
13. Cambier S., Benard G., Mesmer-Dudons N., Gonzalez P., Rossignol R., Brethes D., Bourdineaud J.P. At environmental doses, dietary methylmercury inhibits mitochondrial energy metabolism in skeletal muscles of the zebra fish (Danio rerio). International Journal of Biochemistry & Cell Biology 2009, 41:791-799.
14. Cambier S., Gonzalez P., Mesmer-Dudons N., Brethes D., Fujimura M., Bourdineaud J.-P. Effects of dietary methylmercury on the zebrafish brain: histological, mitochondrial, and gene transcription analyses. Biometals 2012, 25:165-180.
15. Carvalho C.M.L., Chew E.-H., Hashemy S.I., Lu J., Holmgren A. Inhibition of the human thioredoxin system - a molecular mechanism of mercury toxicity. Journal of Biological Chemistry 2008, 283:11913-11923.
16. Clarkson T.W. The toxicology of mercury. Critical Reviews in Clinical Laboratory Sciences 1997, 34:369-403.
17. Clarkson T.W., Magos L. The toxicology of mercury and its chemical compounds. Critical Reviews in Toxicology 2006, 36:609-662.
18. Crump K.L., Trudeau V.L. Mercury-induced reproductive impairment in fish. Environmental Toxicology and Chemistry 2009, 28:895-907.
19. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., Lempicki R.A. DAVID: database for annotation, visualization, and integrated discovery. Genome Biology 2003, 4.
20. Denslow N.D., Garcia-Reyero N., Barber D.S. Fish 'n' chips: the use of microarrays for aquatic toxicology. Molecular Biosystems 2007, 3:172-177.
21. Di Simplicio P., Gorelli M., Ciuffreda P., Leonzio C. The relationship between gamma-glutamyl transpeptidase and Hg levels in Se/Hg antagonism in mouse liver and kidney. Pharmacological Research 1990, 22:515-526.
22. Drew R.E., Rodnick K.J., Settles M., Wacyk J., Churchill E., Powell M.S., Hardy R.W., Murdoch G.K., Hill R.A., Robison B.D. Effect of starvation on transcriptomes of brain and liver in adult female zebrafish (Danio rerio). Physiological Genomics 2008, 35:283-295.
23. Dutczak W.J., Ballatori N. Transport of the glutathione-methylmercury complex across liver canalicular membranes on reduced glutathione carriers. Journal of Biological Chemistry 1994, 269:9746-9751.
24. Dysvik B., Jonassen I. J-Express: exploring gene expression data using Java. Bioinformatics 2001, 17:369-370.
25. Eddy S.R. A new generation of homology search tools based on probabilistic inference. Genome Informatics 2009, 23:205-211.
26. Edvardsen R.B., Malde K., Mittelholzer C., Taranger G.L., Nilsen F. EST resources and establishment and validation of a 16 k cDNA microarray from Atlantic cod (Gadus morhua). Comparative Biochemistry and Physiology D: Genomics & Proteomics 2011, 6:23-30.
27. Ekins S., Bugrim A., Brovold L., Kirillov E., Nikolsky Y., Rakhmatulin E., Sorokina S., Ryabov A., Serebryiskaya T., Melnikov A., Metz J., Nikolskaya T. Algorithms for network analysis in systems-ADME/Tox using the MetaCore and MetaDrug platforms. Xenobiotica 2006, 36:877-901.
28. Ercal N., Gurer-Orhan H., Aykin-Burns N. Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Current Topics in Medicinal Chemistry 2001, 1:529-539.
29. Farina M., Aschner M., Rocha J.B.T. Oxidative stress in MeHg-induced neurotoxicity. Toxicology and Applied Pharmacology 2011, 256:405-417.
30. Garcia-Reyero N., Griffitt R.J., Liu L., Kroll K.J., Farmerie W.G., Barber D.S., Denslow N.D. Construction of a robust microarray from a non-model species largemouth bass, Micropterus salmoides (Lacepede), using pyrosequencing technology. Journal of Fish Biology 2008, 72:2354-2376.
31. Gardner R.M., Nyland J.F., Evans S.L., Wang S.B., Doyle K.M., Crainiceanu C.M., Silbergeld E.K. Mercury induces an unopposed inflammatory response in human peripheral blood mononuclear cells in vitro. Environmental Health Perspectives 2009, 117:1932-1938.
32. Gerk P.M., Vore M. Regulation of expression of the multidrug resistance associated protein 2 (MRP2) and its role in drug disposition. Journal of Pharmacology and Experimental Therapeutics 2002, 302:407-415.
33. Glover C.N., Zheng D., Jayashankar S., Sales G.D., Hogstrand C., Lundebye A.-K. Methylmercury speciation influences brain gene expression and behavior in gestationally-exposed mice pups. Toxicological Sciences 2009, 110:389-400.
34. Goksøyr A., Andersson T., Hansson T., Klungsøyr J., Zhang Y., Förlin L. Species characteristics of the hepatic xenobiotic and steroid biotransformation systems of two teleost fish, Atlantic cod (Gadus morhua) and rainbow trout (Salmo gairdneri). Toxicology and Applied Pharmacology 1987, 89:347-360.
35. Goksøyr A., Beyer J., Husøy A.M., Larsen H.E., Westrheim K., Wilhelmsen S., Klungsøyr J. Accumulation and effects of aromatic and chlorinated hydrocarbons in juvenile Atlantic cod (Gadus morhua) caged in a polluted fjord (Sørfjorden, Norway). Aquatic Toxicology 1994, 29:21-35.
36. Gonzalez P., Dominique Y., Massabuau J.C., Boudou A., Bourdineaud J.P. Comparative effects of dietary methylmercury on gene expression in liver, skeletal muscle, and brain of the zebrafish (Danio rerio). Environmental Science & Technology 2005, 39:3972-3980.
37. Hahn M.E. Mechanistic research in aquatic toxicology: perspectives and future directions. Aquatic Toxicology 2011, 105:67-71.
38. Harada M. Minamata disease: methylmercury poisoning in Japan caused by environmental pollution. Critical Reviews in Toxicology 1995, 25:1-24.
39. Havarinasab S., Hultman P. Organic mercury compounds and autoimmunity. Autoimmunity Reviews 2005, 4:270-275.
40. Jayashankar S., Glover C.N., Folven K.I., Brattelid T., Hogstrand C., Lundebye A.-K. Cerebral gene expression in response to single or combined gestational exposure to methylmercury and selenium through the maternal diet. Cell Biology and Toxicology 2011, 27:181-197.
41. Jensen S., Jernelov A. Biological methylation of mercury in aquatic organisms. Nature 1969, 223:753.
42. Kala S.V., Neely M.W., Kala G., Prater C.I., Atwood D.W., Rice J.S., Lieberman M.W. The MRP2/cMOAT transporter and arsenic-glutathione complex formation are required for biliary excretion of arsenic. Journal of Biological Chemistry 2000, 275:33404-33408.
43. Kensler T.W., Wakabayash N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annual Review of Pharmacology and Toxicology 2007, 89-116.
44. Kramer V.J., Newman M.C., Ultsch G.R. Changes in concentrations of glycolysis and Krebs cycle metabolites in mosquitofish, Gambusia holbrooki, induced by mercuric chloride and starvation. Environmental Biology of Fishes 1992, 34:315-320.
45. Kromidas L., Trombetta L.D., Jamall I.S. The protective effects of glutathione against methylmercury cytotoxicity. Toxicology Letters 1990, 51:67-80.
46. La Fontaine S., Mercer J.F.B. Trafficking of the copper-ATPases, ATP7A and ATP7B: role in copper homeostasis. Archives of Biochemistry and Biophysics 2007, 463:149-167.
47. Lie K.K., Lanzen A., Breilid H., Olsvik P.A. Gene expression profiling in Atlantic cod (Gadus morhua L.) from two contaminated sites using a custom made cDNA microarray. Environmental Toxicology and Chemistry 2009, 28:1711-1721.
48. Lu S.C. Regulation of hepatic glutathione synthesis: current concepts and controversies. FASEB Journal 1999, 13:1169-1183.
49. Meier S., Andersen T.E., Norberg B., Thorsen A., Taranger G.L., Kjesbu O.S., Dale R., Morton H.C., Klungsøyr J., Svardal A. Effects of alkylphenols on the reproductive system of Atlantic cod (Gadus morhua). Aquatic Toxicology 2007, 81:207-218.
50. Moszczynski P. Mercury compounds and the immune system: a review. International Journal of Occupational and Environmental Health 1997, 10:247-258.
51. Ni M., Li X., Yin Z., Jiang H., Sidoryk-Wegrzynowicz M., Milatovic D., Cai J., Aschner M. Methylmercury induces acute oxidative stress, altering Nrf2 protein level in primary microglial cells. Toxicological Sciences 2010, 116:590-603.
52. NRC Toxicological Effects of Methylmercury 2000, The National Academies Press.
53. Nøstbakken O.J., Martin S.A.M., Cash P., Torstensen B.E., Amlund H., Olsvik P.A. Dietary methylmercury alters the proteome in Atlantic salmon (Salmo salar) kidney. Aquatic Toxicology 2012, 108:70-77.
54. Okamuraikeda K., Ikeda Y., Tanaka K. An essential cysteine residue located in the vicinity of the FAD-binding site in short-chain, medium-chain, and long-chain acyl-CoA dehydrogenases from rat liver mitochondria. Journal of Biological Chemistry 1985, 260:1338-1345.
55. Olsvik P.A., Brattås M., Lie K.K., Goksøyr A. Transcriptional responses in juvenile Atlantic cod (Gadus morhua) after exposure to mercury-contaminated sediments obtained near the wreck of the German WW2 submarine U-864, and from Bergen Harbor, Western Norway. Chemosphere 2011, 83:552-563.
56. Olsvik P.A., Lie K.K., Goksøyr A., Midtun T., Frantzen S., Maage A. Are Atlantic cod in Store Lungegrdsvann, a seawater recipient in Bergen, affected by environmental contaminants? A qRT-PCR survey. Journal of Toxicology and Environmental Health-Part A: Current Issues 2009, 72:140-154.
57. Peterson S.A., Van Sickle J., Herlihy A.T., Hughes R.M. Mercury concentration in fish from streams and rivers throughout the western united states. Environmental Science & Technology 2007, 41:58-65.
58. Richter C.A., Garcia-Reyero N., Martyniuk C., Knoebl I., Pope M., Wright-Osment M.K., Denslow N.D., Tillitt D.E. Gene expression changes in female zebrafish (Danio rerio) brain in response to acute exposure to methylmercury. Environmental Toxicology and Chemistry 2011, 30:301-308.
59. Sandheinrich M.B., Bhavsar S.P., Bodaly R.A., Drevnick P.E., Paul E.A. Ecological risk of methylmercury to piscivorous fish of the Great Lakes region. Ecotoxicology 2011, 20:1577-1587.
60. Shimai S., Satoh H. Behavioral teratology of methylmercury. The Journal of Toxicological Sciences 1985, 10:199-216.
61. Simmons-Willis T.A., Koh A.S., Clarkson T.W., Ballatori N. Transport of a neurotoxicant by molecular mimicry: the methylmercury-l-cysteine complex is a substrate for human L-type large neutral amino acid transporter (LAT) 1 and LAT2. Biochemical Journal 2002, 367:239-246.
62. Star B., Nederbragt A.J., Jentoft S., Grimholt U., Malmstrøm M., Gregers T.F., Rounge T.B., Paulsen J., Solbakken M.H., Sharma A., Wetten O.F., Lanzen A., Winer R., Knight J., Vogel J.-H., Aken B., Andersen Ø., Lagesen K., Tooming-Klunderud A., Edvardsen R.B., Tina K.G., Espelund M., Nepal C., Previti C., Karlsen B.O., Moum T., Skage M., Berg P.R., Gjøen T., Kuhl H., Thorsen J., Malde K., Reinhardt R., Du L., Johansen S.D., Searle S., Lien S., Nilsen F., Jonassen I., Omholt S.W., Stenseth N.C., Jakobsen K.S. The genome sequence of Atlantic cod reveals a unique immune system. Nature 2011, 477:207-210.
63. Stohs S.J., Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radical Biology and Medicine 1995, 18:321-336.
64. Suzek B.E., Huang H., McGarvey P., Mazumder R., Wu C.H. UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 2007, 23:1282-1288.
65. Sweet L.I., Zelikoff J.T. Toxicology and immunotoxicology of mercury: a comparative review in fish and humans. Journal of Toxicology and Environmental Health-Part B: Critical Reviews 2001, 4:161-205.
66. Toyama T., Sumi D., Shinkai Y., Yasutake A., Taguchi K., Tong K.I., Yamamoto M., Kumagai Y. Cytoprotective role of Nrf2/Keap1 system in methylmercury toxicity. Biochemical and Biophysical Research Communications 2007, 363:645-650.
67. Tusher V.G., Tibshirani R., Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:5116-5121.
68. Ung C.Y., Lam S.H., Hlaing M.M., Winata C.L., Korzh S., Mathavan S., Gong Z. Mercury-induced hepatotoxicity in zebrafish: in vivo mechanistic insights from transcriptome analysis, phenotype anchoring and targeted gene expression validation. BMC Genomics 2010, 11.
69. Vogel D.G., Margolis R.L., Mottet N.K. The effects of methyl mercury binding to microtubules. Toxicology and Applied Pharmacology 1985, 80:473-486.
70. Wahli W., Braissant O., Desvergne B. Peroxisome proliferator activated receptors: transcriptional regulators of adipogenesis, lipid metabolism and more. Chemistry & Biology 1995, 2:261-266.
71. Wang R.-L., Bencic D., Villeneuve D.L., Ankley G.T., Lazorchak J., Edwards S. A transcriptomics-based biological framework for studying mechanisms of endocrine disruption in small fish species. Aquatic Toxicology 2010, 98:230-244.
72. Wang T., Hung C.C.Y., Randall D.J. The comparative physiology of food deprivation: from feast to famine. Annual Review of Physiology 2006, 68:223-251.
73. Wolfe M.F., Schwarzbach S., Sulaiman R.A. Effects of mercury on wildlife: a comprehensive review. Environmental Toxicology and Chemistry 1998, 17:146-160.
74. Yoshida E., Toyama T., Shinkai Y., Sawa T., Akaike T., Kumagai Y. Detoxification of methylmercury by hydrogen sulfide-producing enzyme in mammalian cells. Chemical Research in Toxicology 2011, 24:1633-1635.
75. Yu X., Robinson J.F., Sidhu J.S., Hong S., Faustman E.M. A system-based comparison of gene expression reveals alterations in oxidative stress, disruption of ubiquitin-proteasome system and altered cell cycle regulation after exposure to cadmium and methylmercury in mouse embryonic fibroblast. Toxicological Sciences 2010, 114:356-377.